Deregulation of the miR-222-ABCG2 regulatory module in tongue squamous cell carcinoma contributes to chemoresistance and enhanced migratory/invasive potential

Oncotarget

Volumn 6, Issue 42, 2015, Pages 44538-44550

  Zhao, Luodan ^a   Ren, Yuexin ^b   Tang, Haikuo ^a   Wang, Wei ^a   He, Qianting ^a   Sun, Jingjing ^a   Zhou, Xiaofeng ^c   Wang, Anxun ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

ABCG2; Chemoresistance; Cisplatin; Metastasis; Tongue squamous cell carcinoma

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CISPLATIN; COMPLEMENTARY DNA; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; MICRORNA 222; ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; MICRORNA; MIRN222 MICRORNA, HUMAN; TUMOR PROTEIN;

ABCG2 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER RESISTANCE; CELL INVASION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG EFFECT; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; TONGUE CARCINOMA; TUMOR INVASION; ANIMAL; BAGG ALBINO MOUSE; CARCINOMA, SQUAMOUS CELL; CELL MOTION; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HEAD AND NECK NEOPLASMS; IC50; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SECONDARY; TIME FACTOR; TONGUE NEOPLASMS; TUMOR CELL CULTURE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 2; ATP-BINDING CASSETTE TRANSPORTERS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; CISPLATIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; INHIBITORY CONCENTRATION 50; LUNG NEOPLASMS; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TONGUE NEOPLASMS; TRANSFECTION; TUMOR BURDEN; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84953432115     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6253     Document Type: Article

References (44)

1. Price KA, Cohen EE. Current treatment options for metastatic head and neck cancer. Curr Treat Options Oncol. 2012; 13:35-46.
2. Yu ZW, Zhong LP, Ji T, Zhang P, Chen WT, Zhang CP. MicroRNAs contribute to the chemoresistance of cisplatin in tongue squamous cell carcinoma lines. Oral Oncol. 2010; 46:317-322.
3. Nguyen-Tan PF, Zhang Q, Ang KK, Weber RS, Rosenthal DI, Soulieres D, Kim H, Silverman C, Raben A, Galloway TJ, Fortin A, Gore E, Westra WH, et al. Randomized phase III trial to test accelerated versus standard fractionation in combination with concurrent cisplatin for head and neck carcinomas in the Radiation Therapy Oncology Group 0129 trial: long-term report of efficacy and toxicity. J Clin Oncol. 2014; 32:3858-3866.
4. Gungor C, Zander H, Effenberger KE, Vashist YK, Kalinina T, Izbicki JR, Yekebas E, Bockhorn M. Notch signaling activated by replication stress-induced expression of midkine drives epithelial-mesenchymal transition and chemoresistance in pancreatic cancer. Cancer Res. 2011; 71:5009-5019.
5. Chen X, Lingala S, Khoobyari S, Nolta J, Zern MA, Wu J. Epithelial mesenchymal transition and hedgehog signaling activation are associated with chemoresistance and invasion of hepatoma subpopulations. J Hepatol. 2011; 55:838-845.
6. Liu M, Wang J, Huang H, Hou J, Zhang B, Wang A. miR-181a-Twist1 pathway in the chemoresistance of tongue squamous cell carcinoma. Biochem Biophys Res Commun. 2013; 441:364-370.
7. Gong W, Wang Z, Wan Y, Shi L, Zhou Y. Downregulation of ABCG2 protein inhibits migration and invasion in U251 glioma stem cells. Neuroreport.2014; 25:625-632.
8. Zhu Y, Liu XJ, Yang P, Zhao M, Lv LX, Zhang GD, Wang Q, Zhang L. Alkylglyceronephosphate synthase (AGPS) alters lipid signaling pathways and supports chemotherapy resistance of glioma and hepatic carcinoma cell lines. Asian Pac J Cancer Prev. 2014; 15:3219-3226.
9. Huang L, Lu Q, Han Y, Li Z, Zhang Z, Li X. ABCG2/V-ATPase was associated with the drug resistance and tumor metastasis of esophageal squamous cancer cells.DiagnPathol. 2012;7:180.
10. Yanamoto S, Kawasaki G, Yamada S, Yoshitomi I, Kawano T, Yonezawa H, Rokutanda S, Naruse T, Umeda M. Isolation and characterization of cancer stem-like side population cells in human oral cancer cells. Oral Oncol. 2011; 47:855-860.
11. Lopez JP, Wang-Rodriguez J, Chang C, Chen JS, Pardo FS, Aguilera J, Ongkeko WM. Gefitinib inhibition of drug resistance to doxorubicin by inactivating ABCG2 in thyroid cancer cell lines. Arch Otolaryngol Head Neck Surg. 2007; 133:1022-1027.
12. Xie ZY, Lv K, Xiong Y, Guo WH. ABCG2-meditated multidrug resistance and tumor-initiating capacity of side population cells from colon cancer. Oncol Res Treat. 2014; 37:666-668, 670-672.
13. Liu X, Yu J, Jiang L, Wang A, Shi F, Ye H, Zhou X. MicroRNA-222 regulates cell invasion by targeting matrix metalloproteinase 1 (MMP1) and manganese superoxide dismutase 2 (SOD2) in tongue squamous cell carcinoma cell lines. Cancer Genomics Proteomics. 2009; 6:131-139.
14. Chen Z, Jin Y, Yu D, Wang A, Mahjabeen I, Wang C, Liu X, Zhou X. Down-regulation of the microRNA-99 family members in head and neck squamous cell carcinoma. Oral Oncol. 2012; 48:686-691.
15. He Q, Zhou X, Li S, Jin Y, Chen Z, Chen D, Cai Y, Liu Z, Zhao T, Wang A. MicroRNA-181a suppresses salivary adenoid cystic carcinoma metastasis by targeting MAPK-Snai2 pathway. Biochim Biophys Acta. 2013; 1830:5258-5266.
16. Chen D, Chen Z, Jin Y, Dragas D, Zhang L, Adjei BS, Wang A, Dai Y, Zhou X. MicroRNA-99 family members suppress Homeobox A1 expression in epithelial cells. Plos One. 2013; 8:e80625.
17. Jiang L, Liu X, Chen Z, Jin Y, Heidbreder CE, Kolokythas A, Wang A, Dai Y, Zhou X. MicroRNA-7 targets IGF1R (insulin-like growth factor 1 receptor) in tongue squamous cell carcinoma cells. Biochem J. 2010; 432:199-205.
18. Liu X, Wang A, Heidbreder CE, Jiang L, Yu J, Kolokythas A, Huang L, Dai Y, Zhou X. MicroRNA-24 targeting RNA-binding protein DND1 in tongue squamous cell carcinoma. FEBS Lett. 2010; 584:4115-4120.
19. Shen WW, Zeng Z, Zhu WX, Fu GH. MiR-142-3p functions as a tumor suppressor by targeting CD133, ABCG2, and Lgr5 in colon cancer cells. J Mol Med (Berl). 2013; 91:989-1000.
20. Shi L, Wang Z, Sun G, Wan Y, Guo J, Fu X. miR-145 inhibits migration and invasion of glioma stem cells by targeting ABCG2. Neuromolecular Med. 2014; 16:517-528.
21. Ma MT, He M, Wang Y, Jiao XY, Zhao L, Bai XF, Yu ZJ, Wu HZ, Sun ML, Song ZG, Wei MJ. MiR-487a resensitizes mitoxantrone (MX)-resistant breast cancer cells (MCF-7/MX) to MX by targeting breast cancer resistance protein (BCRP/ABCG2). Cancer Lett. 2013; 339:107-115.
22. Peng F, Zhang H, Du Y, Tan P. miR-23a promotes cisplatin chemoresistance and protects against cisplatin-induced apoptosis in tongue squamous cell carcinoma cells through Twist. Oncol Rep. 2015; 33:942-950.
23. Santiskulvong C, Konecny GE, Fekete M, Chen KY, Karam A, Mulholland D, Eng C, Wu H, Song M, Dorigo O. Dual targeting of phosphoinositide 3-kinase and mammalian target of rapamycin using NVP-BEZ235 as a novel therapeutic approach in human ovarian carcinoma. ClinCancer Res. 2011; 17:2373-2384.
24. Yashiro M, Nishii T, Hasegawa T, Matsuzaki T, Morisaki T, Fukuoka T, Hirakawa K. A c-Met inhibitor increases the chemosensitivity of cancer stem cells to the irinotecan in gastric carcinoma. Br J Cancer. 2013; 109:2619-2628.
25. Song W, Jiang R, Zhao CM. Role of integrin-linked kinase in multi-drug resistance of human gastric carcinoma SGC7901/DDP cells. Asian Pac J Cancer Prev. 2012; 13:5619-5625.
26. Yang JM, Xu Z, Wu H, Zhu H, Wu X, Hait WN. Overexpression of extracellular matrix metalloproteinase inducer in multidrug resistant cancer cells. Mol Cancer Res. 2003; 1:420-427.
27. Vaidya KS, Sanchez JJ, Kim EL, Welch DR. Expression of the Breast Cancer Metastasis Suppressor 1 (BRMS1) maintains in vitro chemosensitivity of breast cancer cells. Cancer Lett. 2009; 281:100-107.
28. Hoshino H, Miyoshi N, Nagai K, Tomimaru Y, Nagano H, Sekimoto M, Doki Y, Mori M, Ishii H. Epithelial-mesenchymal transition with expression of SNAI1-induced chemoresistance in colorectal cancer. Biochem Biophys Res Commun. 2009; 390:1061-1065.
29. Zhu L, Hu Z, Liu J, Gao J, Lin B. Gene expression profile analysis identifies metastasis and chemoresistance-associated genes in epithelial ovarian carcinoma cells. Med Oncol. 2015; 32:426.
30. Volk-Draper L, Hall K, Griggs C, Rajput S, Kohio P, DeNardo D, Ran S. Paclitaxel therapy promotes breast cancer metastasis in a TLR4-dependent manner. Cancer Res. 2014; 74:5421-5434.
31. Maseki S, Ijichi K, Tanaka H, Fujii M, Hasegawa Y, Ogawa T, Murakami S, Kondo E, Nakanishi H. Acquisition of EMT phenotype in the gefitinib-resistant cells of a head and neck squamous cell carcinoma cell line through Akt/GSK-3beta/snail signalling pathway. Br J Cancer. 2012; 106:1196-1204.
32. Rosano L, Cianfrocca R, Spinella F, Di Castro V, Nicotra MR, Lucidi A, Ferrandina G, Natali PG, Bagnato A. Acquisition of chemoresistance and EMT phenotype is linked with activation of the endothelin A receptor pathway in ovarian carcinoma cells. Clin Cancer Res. 2011; 17:2350-2360.
33. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R, Gray MJ, Cheng H, Hoff PM, Ellis LM. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res. 2006; 12:4147-4153.
34. Wang X, Xia B, Liang Y, Peng L, Wang Z, Zhuo J, Wang W, Jiang B. Membranous ABCG2 expression in colorectal cancer independently correlates with shortened patient survival. Cancer Biomark. 2013; 13:81-88.
35. Yanamoto S, Yamada S, Takahashi H, Naruse T, Matsushita Y, Ikeda H, Shiraishi T, Seki S, Fujita S, Ikeda T, Asahina I, Umeda M. Expression of the cancer stem cell markers CD44v6 and ABCG2 in tongue cancer: effect of neoadjuvant chemotherapy on local recurrence. Int J Oncol.2014; 44:1153-1162.
36. Qiao B, Johnson NW, Chen X, Li R, Tao Q, Gao J. Disclosure of a stem cell phenotype in an oral squamous cell carcinoma cell lineinduced by BMP-4 via an epithelial-mesenchymal transition. Oncol Rep. 2011; 26:455-461.
37. Ye H, Wang A, Lee BS, Yu T, Sheng S, Peng T, Hu S, Crowe DL, Zhou X. Proteomic based identification of manganese superoxide dismutase 2 (SOD2) as a metastasis marker for oral squamous cell carcinoma. Cancer Genomics Proteomics. 2008; 5:85-94.
38. Ye H, Yu T, Temam S, Ziober BL, Wang J, Schwartz JL, Mao L, Wong DT, Zhou X. Transcriptomic dissection of tongue squamous cell carcinoma. BMC Genomics. 2008; 9:69.
39. Zhou S, Zhang S, Wang Y, Yi S, Zhao L, Tang X, Yu B, Gu X, Ding F. MiR-21 and miR-222 inhibit apoptosis of adult dorsal root ganglion neurons by repressing TIMP3 following sciatic nerve injury. Neurosci Lett. 2015; 586:43-49.
40. Zhang Y, Yao J, Huan L, Lian J, Bao C, Li Y, Ge C, Li J, Yao M, Liang L, He X. GNAI3 inhibits tumor cell migration and invasion and is post-transcriptionally regulated by miR-222 in hepatocellular carcinoma. Cancer Lett. 2015; 356:978-984.
41. Zhou Z, Zheng C, Li S, Zhou X, Liu Z, He Q, Zhang N, Ngan A, Tang B, Wang A. AFM nanoindentation detection of the elastic modulus of tongue squamous carcinoma cells with different metastatic potentials. Nanomedicine.2013; 9:864-874.
42. Gioanni J, Fischel JL, Lambert JC, Demard F, Mazeau C, Zanghellini E, Ettore F, Formento P, Chauvel P, Lalanne CM, Courdi A. Two new human tumor cell lines derived from squamous cell carcinomas of the tongue: establishment, characterization and response to cytotoxic treatment. Eur J Cancer Clin Oncol. 1988; 24:1445-1455.
43. Chang B, Li S, He Q, Liu Z, Zhao L, Zhao T, Wang A. Deregulation of Bmi-1 is associated with enhanced migration, invasion and poor prognosis in salivary adenoid cystic carcinoma. Biochim Biophys Acta. 2014; 1840:3285-3291.
44. Jin Y, Chen Z, Liu X, Zhou X. Evaluating the microRNA targeting sites by luciferase reporter gene assay. Methods Mol Biol. 2013; 936:117-127.